ALLELOPATHIC IMPACTS OF

SCHINUS MOLLE (PERUVIAN PEPPER )

ON INVASVIE AND NATIVE COMMUNITIES

OF SOUTHERN CALIFORNIA

A Thesis

Presented to the

Faculty of

California State Polytechnic University, Pomona

In Partial Fulfillment

Of the Requirements for the Degree

Master of Science

In

Regenerative Studies

By

David C. Bañuelas

2018

SIGNATURE PAGE

THESIS: ALLELOPATHIC IMPACTS OF MOLLE (PERUVIAN PEPPER TREE) ON INVASIVE AND NATIVE PLANT COMMUNITIES OF SOUTHERN CALIFORNIA

AUTHOR: David C. Bañuelas

DATE SUBMITTED: Spring 2018

Lyle Center for Regenerative Studies

Dr. Edward G. Bobich Thesis Committee Chair Biological Sciences

Dr. Erin J. Questad Biological Sciences

Dr. Kristen Conway-Gómez Geography & Anthropology

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ACKNOWLEDGEMENTS

I would first like to thank the thesis committee in their tireless efforts to support my research. Dr. Questad especially, as she provided the constructive atmosphere to pursue my scientific interests and has been a dedicated and trusted adviser. Dr. Bobich, having also taught at Whittier College, was suggested to me as a potential committee member when I graduated from Whittier in 2013. Since starting the Regenerative Studies

(MSRS) program in 2016, I am so grateful for the advice and the opportunity to work with Dr. Bobich. Also, in 2013 I had the privilege of meeting Dr. Conway-Gómez in her

GIS certificate program. Although I became more than familiar with GIS, what I would learn about “community” in her MSRS course would be even more valuable. I owe a tremendous debt of gratitude to my committee as they have been the greatest influence in my life to pursue a PhD at UC Irvine.

I am also grateful for the following people: Dr. La Roche and Dr. Lawrence for always supporting my research and everyone at the Lyle Center. To my 2016 cohort, thank you so much for the love and late nights in the grad-studio. Jennifer Alexander was huge in helping me set up my experiment on the roof top of building 8. Everyone at the

CNPS South Coast Chapter. Dr. Bahr and Ms. Bejarano-Vera from the MENTORES program, who selected me for their scholarship. Everyone at the Garden Club of

America, who provided the funding for my project. The members of the Questad lab where amazing and provided so many great memories and assistance. To Randall Lewis,

Ksenia Glenn, and Dr. Kelly of the Upland Unified School District who provided amazing employment during my graduate studies. Lastly, I am grateful to my family and

Jonaé Varela for without her love and support I would not be here today!

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ABSTRACT

Since (California pepper tree) was introduced to Southern

California in 1830, it has escaped ornamental cultivation becoming invasive. Prior to this study, it had not been had determined if S. molle possess the same potential for allelopathy or a legacy effect in California as does S. terebinthifolius in Florida.

However, S. molle is known to be allelopathic against crops and associated weeds. In

Mexico, litter and soil of S. molle exhibits stronger chemical inhibition than females.

The first objective of this study, therefore, was to find the role of S. molle in restoration, specifically if chemical inhibition is selective against native or non-native plant species.

Secondly, we sought to uncover any differential allelopathy amongst both sexes of S. molle. Two separate experiments were conducted to investigate S. molle allelopathy and potential legacy effect. The first applied mulches from both genders of S. molle to three native and three invasive plant species. The second experiment sowed the same species in soil collected from both sexes of S. molle. We expected the male mulch (staminate and ) and soil would have a greater inhibitory effect on native and non-native species compared to the control. The results of this study found male pepper tree mulch stimulated shoot growth in four out of six species tested (A. intermedia, B. nigra,

B. madritensis, and S. pulchra) and did not have a strong effect on germination. Nor did this study find strong evidence that S. molle and S. terebinthifolius share the same impetus for allelopathy or legacy effects. In fact, S. molle may facilitate native understory plants based on field observations in three locations. Thus, our study highlights the need of future research to determine the role of both genders in restoration and management.

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TABLE OF CONTENTS

SIGNATURE PAGE ...... ii ACKNOWLEDGEMENTS ...... iii ABSTRACT ...... iv LIST OF TABLES ...... vi LIST OF FIGURES ...... vii INTRODUCTION...... 1 MATERIALS AND METHODS ...... 6 RESULTS ...... 11 DISCUSSION ...... 14 CONCLUSION ...... 19 TABLES AND FIGURES ...... 20 REFERENCES ...... 31

.

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LIST OF TABLES

Table 1. Summary for mulch experiement ...... 21

Table 2. Summary for soil experiement ...... 22

Table 3. List of plant species found in field transects...... 30

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LIST OF FIGURES

Figure 1. Map of field observations ...... 20

Figure 2. Percent shoot emergence of mulch experiement ...... 23

Figure 3. Mulch root biomass per individual ...... 24

Figure 4. Mulch shoot biomass per individual...... 25

Figure 5. Percent shoot emergence of soil experiement ...... 26

Figure 6. Soil root biomass per individual ...... 27

Figure 7. Soil shoot biomass per individual...... 28

Figure 8. Volumetric soil water content ...... 29

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INTRODUCTION

In the United States, non-native, highly invasive plants require billions of dollars annually for their control and eradication (Pimentel et al., 2005). Invasive plants and pathogens are responsible for reductions in crop yields of 10-40% worldwide (Fried et al., 2017), and exacerbate conditions for the displacement and local extinction of native plant species (Hobbs, 2000). Endemic plant communities are especially vulnerable, having no prior evolutionary exposure to non-native species (Pyšek et al., 2017). Traits, such as superior drought tolerance or rapid seed dispersal, can give invasive species a competitive advantage (Callaway & Ridenour, 2004). In the endemic plant communities of Southern California, the invasion and establishment of non-native species are aided by anthropogenic disturbance and nitrogen deposition (Larios et al., 2017; Stylinski & Allen,

1999; Valliere et al., 2017). One of the lesser understood mechanisms that fuels plant invasions is the ability of certain species to influence others through allelopathy

(Dawkins & Esiobu, 2016).

Allelopathic compounds produced through secondary metabolic pathways in plants can negatively impact other plant species, as well as algae, bacteria, and fungi, in agricultural or natural systems (Chou, 2006). Allelopathy can aid plant species in resource competition, mostly by inhibiting the growth and germination of neighboring species (Rice, 1984). Schinus terebinthifolius R. (Brazilian pepper tree), which was

introduced as an ornamental species, is invasive and allelopathic, naturalizing and

displacing native species since it was brought intentionally to the Florida Everglades in

1898 (Cuda et al., 2006; Donnelly et al., 2008; Morgan & Overholt, 2005; Morton, 1978;

Nickerson & Flory, 2015). Where it occurs in mangroves, S. terebinthifolius leaf litter

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causes extensive dieback for native mangroves; such dieback is amplified in higher salinity (Donnelly et al., 2008). Thus, invasive species can reduce populations of native species through direct allelopathy.

Invasive species can also have a negative effect on the growth and germination of native plants indirectly through alterations in the rhizosphere. The soil microbiota associated with S. terebinthifolius has a higher relative abundance of arbuscular fungi and fewer species of pathogenic fungi when compared to the soil of intact native communities

(Dawkins & Esiobu, 2017). Other species, like yellow star thistle (Centaurea solstitialis), change the microbiota of the rhizosphere by promoting the growth of sulfur-oxidizing and sulfur-reducing bacteria (Batten et al., 2006). Yellow star thistle can also outcompete native species for resources, as evidenced by the fact that it depletes soil moisture faster than native grasses (Enloe et al., 2004). Diffuse knapweed (Centaurea diffusa), a common range pest, secretes an antibacterial compound (8-hydroxy-quinolone) to alter the rhizosphere (Callaway et al., 2004). , an invasive throughout

California, produces glucosinolates in soil, preventing the establishment of native species by inhibiting the growth of arbuscular fungi (Aprahamian et al., 2016; Maltz et al., 2016).

These effects can remain in the soil despite the removal or defoliation of the invasive species, thus creating a “legacy” effect (Corbin & D’antonio, 2012; Dawkins & Esiobu,

2016).

Understanding the negative effects from soil legacies and allelopathy is crucial to invasive species management and native plant restoration. Much of California’s native grasslands for example, have been replaced by annual invasive grasses from the

Mediterranean (Bartolome et al., 2013; Larios et al., 2017). Two annual invasive grasses,

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Elymus caput-medusae (Medusahead) and Aegilops triuncialis (Barb goatgrass) decrease the presence of available soil nitrogen, which can stifle the recovery of native grasses

(Carey et al., 2017). Native annual forbs are also negatively affected by invasive grasses and are a crucial component of native grasslands. For instance, Phacelia distans and

Amsinkia intermedia can establish by seeding and removing invasive grasses, but will only increase in abundance during years with favorable precipitation, rendering treatments indistinguishable following seasons with low rainfall (Thomson et al., 2016;

Thomson et al., 2018). As a result of drought and disturbance, both native annual forbs and perennial grasses become seed limited, which facilitates the establishment of invasive grasses (Seabloom et al., 2003a, 2003b). Therefore, future management strategies need lasting results that insulate native species from less favorable conditions and mitigate impacts from allelopathy and legacy effects.

This study was performed to assess the allelopathy from litter and potential soil legacy effect left by Schinus molle L. (Peruvian or California pepper tree; Anacardaciae).

The pepper tree was first introduced to California from in 1830 (Kramer, 1957). Its widespread use as an ornamental street tree in Southern California enabled its naturalization into native and invaded plant communities (Howard & Minnich, 1989;

Nilsen & Muller, 1980). Regionally, the impact of S. molle on native plant species is still unknown, but its ability to invade is deemed “limited” by the California Invasive Plant

Council (Cal-IPC) (Cal-IPC, 2006). The species has also escaped cultivation elsewhere, leading to its naturalization in Tunisia, Australia, Spain, Mexico, and South Africa, where its impact is most severe (Avendaño-González et al., 2016; Blood, 2001; Ennigrou et al.,

2011; Godoy et al., 2011; Iponga et al., 2008; Miller et al., 2010).

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In South Africa, urban forests provide the seed stock for dispersal of S. molle by avian fauna as well as the Chacma baboon (Papio ursinus) in disturbed locations and in microsites beneath native and invasive (Iponga et al., 2009, 2010; Shackleton &

Shackleton, 2016; Tew et al., 2018). Indigenous species near S. molle are smaller due to the fact that they are out-competed for light, and thus suffer greater branch die-off and diminished seed production compared to what is typical for those species (Iponga et al.,

2008; Iponga et al., 2009). No study has yet determined if S. molle has similar and/or allelopathic impacts on native plant communities in California. Similarly, no previous research has identified specific pathways for legacy effects of S. molle like those of S. terebinthifolius. Soil beneath S. molle appears to affect establishment of other species. In fact, soil collected beneath the canopies of male and female trees inhibited the germination and biomass of six cactus species native to northern Mexico (Avendaño-

González et al., 2016). Previous studies on S. molle allelopathy primarily focused on the female , which are thought to have higher concentrations of terpenes (Anaya &

Gómez-Pompa, 1971; Borella et al., 2011; Materechera et al., 2008; Pawlowski et al.,

2012; Zahed et al., 2010). However, five of six succulent species native to the

Chihuahuan Desert experienced greater reductions in germination and biomass when exposed to extracts and soil from male S. molle compared to those from females

(Avendaño-González et al., 2016).

Because pepper trees are dioecious, chemical differences between genders

(Garzoli et al., 2018), could provide several options for invasive species management and native plant restoration. Aqueous extracts from S. molle can reduce the germination and growth of wheat (Triticum sativa), as well as weeds in manure-amended soil using female

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fruits and leaves (Materechera et al., 2008). Comparing fruits and female leaves against staminate and male leaves in future studies could elucidate possible pathways for pepper tree applications to be selective against invasive species. While many allelopathic species have been deployed to suppress agricultural pests, there is limited focus on utilizing allelopathic trees to treat other invasive species for native plant restoration

(Amri et al., 2013; Ashraf et al., 2017; Nagabhushana et al., 2001). If native species can tolerate either female or male pepper trees and certain invasive species cannot, native plants could be planted near or beneath the canopy of pepper trees or in association with pepper tree mulch for restoration.

The first objective of this thesis project was to assess the viability of such an approach and its impact on native and invasive plant species. The second objective was to uncover differential allelopathy amongst male and female pepper trees, including their separate legacy effects. Two experiments were used to carry out the research objectives.

The first experiment determined how mulch from male and female trees affected both native and invasive species. The second experiment tested the potential soil legacy effects of both genders and whether they had the potential to inhibit the germination of three native and three invasive species. I hypothesized that S. molle are non-selective and would reduce the germination and dry biomass of all six species. Furthermore, I expected that soil under and mulch made from male plants would be more allelopathic than soil under and mulch made from female plants, as found by Avendaño-González et al. (2016).

The results of this study were the first step in determining the potential use of pepper trees in restoration. Additionally, this study elucidated any differential allelopathy on native and invasive plant species in Southern California.

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MATERIALS AND METHODS

Site Description

The leaf litter of and soil beneath Schinus molle used for the experiment were collected from the Voorhis Ecological Reserve (VER) on the California State Polytechnic

University campus, Pomona (34° 3'31.29"N, 117°49'49.84"W). The city of Pomona has an annual mean temperature of 17.0 °C and averages 431 mm of precipitation per year

(Pomona Fairplex, WRCC, 2016). In the 31-ha reserve, S. molle was most likely introduced from landscaping when the campus was developed in 1956 (Pearson &

Stebbins, 1977). The two experiments in this study were conducted between September

2017 and April 2018 on the rooftop of Building 8 (Science).

Plant Material

Seeds of Bromus madritensis (foxtail brome), Silybum marianum (milk thistle), and Brassica nigra (black ), all of which are invasive and greatly impact native plant communities (Cal-IPC, 2006), were collected in the VER between May and August

2017. Seeds from native forbs, Amsinkia intermedia and Phacelia ramosissima, along with one native perennial grass, Stipa pulchra, where purchased from S & S Seeds, Inc.

(Carpinteria, CA). They were collected in the Counties of Los Angeles and Riverside between 2014-2017. The native species were selected based on their ease of germination in greenhouse settings and their importance towards restoration in the VER (Lauman personal communication, 2017).

Mulch Treatment

To assess how invasive and native species respond to applications of pepper tree mulch, four treatments and a control were used. Two pepper tree treatments included one

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consisting of mulch made from the material of male plants and the other from material of female plants. For the mulch treatment, five trees from each gender were randomly selected in the VER. Staminate flowers (with stems) and leaves were collected from each male specimen. Likewise, unripe fruits still attached to the stem and leaves were collected from each female tree. The pepper tree material was collected four days prior to experiment planting, rinsed with distilled water, and dried for four days at room temperature. Although rinsing may remove allelopathic compounds, this study followed previous methods, in which material was rinsed to remove particulate matter that could originate from urban areas (Avendaño-González et al., 2016).

All treatments and the control were performed in 25 cm square seedling flats and filled with 3 L of general use potting soil (Pro-Mix® BX, Saint-Antonin, QC, Canada).

For each species assessed, five flats were assigned as replicates for each treatment (5 flats x 4 treatments = 20 flats per species). For A. intermedia, B. madritensis, P. ramosissima,

S. marianum, and S. pulchra, 20 seeds were sown per flat (20 seeds x 5 flats = 100), and

100 seeds per flat were sown for B. nigra to account for low seed viability (100 x 5 flats

= 500 seeds per mulch type). Seeds were sown prior to application of mulch treatments with trays arranged randomly under a shaded-outdoor area. For each tray receiving male mulch, 30 g of male leaves and 30 g of staminate flowers with stems were used.

Similarly, the female mulch was applied using 30 g of leaf material and 30 g of crushed fruits in each tray; fruits were crushed to prevent germination. To determine the effects of cover, non-allelopathic mulch (control) was applied to each tray using 60 g of dry coconut shells (PlantBest Mega Mulch™) in addition to a control with no mulch.

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Germination was recorded weekly for A. intermedia, B. madritensis, S. marianum, and S. pulchra, and sown between October and December 2017. Seed germination was assessed every day for the first 30 d and every other day thereafter for P. ramosissima and B. nigra. Each flat was watered to field capacity daily for 30 d and every other day for the remainder of the experiment. Successful germination was assumed when aerial shoots were visible. Both P. ramosissima and B. nigra were sown in the mulch treatments between March and April 2018. To measure the effect of mulch treatments on growth, roots, and shoots from each species were harvested after 50 d, dried in a forced air oven at 60 °C, removed after four days, and weighed in g.

Soil Experiment

The same set of 10 trees (N = 5 each for male and female) used to collect mulch material were used for the soil experiment to study the possible legacy effects of S. molle in restoration. For the control, soil with no vegetation visible at the time of collection was used. 180 L of soil (3 L per flat) were collected beneath the canopy from the five trees of each gender in January 2018 (90 L per gender). For the control, 180 L of soil were collected from an area that had no vegetation and was at least 20 m from any pepper trees. For all three soil types, soil was collected from the top 10 cm and pooled to remove leaf litter, rocks, and other debris.

For each species assessed, five flats were used as replicates for each treatment (5 flats x 3 soil types = 15 flats per species). Twenty seeds were sown per flat for each species (20 seeds x 5 flats = 100 seeds per soil type), except B. nigra, for which 100 were sown per flat (100 x 5 flats = 500). Germination was assessed every day for all species for the first 30 d of the experiment and every other day thereafter. All seedling trays were

8

watered to field capacity every day for first 30 d and every other day for the remainder.

As above, germination was assumed when aerial shoots became visible. After 50 d, all roots and shoots were removed, dried in a forced air oven at 60 °C for 4 d, and weighed in g.

Soil Moisture

To assess differences in soil moisture content amongst mulch treatments, volumetric soil content (ML3 ThetaProbe AT Delta-T Devices, Burwell, Cambridge

CB25 0EJ, UK) was recorded every day for the first 30 days and every other day thereafter during the B. nigra and P. ramosissima mulch trials. Four 3 L round pots were used, each containing the four treatment types and placed near the mulch trial with no seeds planted. Each pot was given the same mulch weight given to six plant species in the mulch trial.

Field Observations

A total of 24 transects of 15 m were sampled between April and May 2018 in the

Chino Hills State Park (33° 55'4.56"N, 117°43'28.49"W), Puente Hills Landfill Native

Habitat Preserve (PHLNHP; 33° 58'20.72"N, 117°59'53.62"W), and the VER (Figure 1).

The transects were conducted beneath the canopies of female and male pepper trees;

Quercus agrifolia (Coast live oak), a native evergreen tree with a comparable canopy spread, and in an area without tree cover that was at least 20 m from any oak tree or any gender of pepper tree. At each location, two female and male pepper trees were randomly selected along with two oak trees. Six transects (2 per location) were recorded in total for all four cover types (female, male, oak, open).

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Each transect was located on slopes that faced 0° north (Figure 1), with the beginning and end of each transect occurring below the dripline of tree cover. At each 15 m transect, a 1×1 m quadrat was placed at every other m to record the occurrence of all species. A total of 192 quadrats (8 per transect) were recorded in 24 transects (6 per cover type). To calculate the percent cover of species in each transect, the sum occurrence for each species was divided individually by the total number of quadrats (48 per cover type). The transects were taken to collect baseline data of the species associated with pepper trees as well as the comparable native tree cover. Each location includes remnant native plant communities that have experienced significant disturbances from development and overgrazing.

Statistical Analysis

A one-way analysis of variance (ANOVA) was used to compare differences in percent shoot emergence, dry biomass of roots and shoots in the mulch, and the soil experiment. To calculate the root and shoot growth means, the number of individuals germinated by the final day of experiment in each tray was divided by the growth weight in g. In the mulch trial, the fixed factor was mulch type with soil type being the fixed factor in the soil experiment. This analysis was carried out individually for each species and a post-hoc Tukey test was used to assess differences among the treatments at the 0.05 level of significance. Statistical analysis was conducted using RStudio Version 1.1.423

(RStudio Inc., Boston, MA, 2015).

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RESULTS

Mulch Experiment

The percent shoot emergence of the perennial forb P. ramosissima was highest in

the coconut mulch at 76% and was 44% in the male mulch (Figure 2C). The percent

shoot emergence of P. ramosissima was slightly lower in the control (no mulch) at 33% and was lowest in the male female mulch at 13% (Figure 2C). Shoot emergence of P. ramosissima was significantly different among all treatments (p < 0.05), except for the percent shoot emergence of the male mulch and control (no mulch; Figure 2C). Shoot emergence of the native perennial grass S. pulchra and the invasive forbs B. nigra and S. marianum was not affected by any treatment. The percent shoot emergence for the native forb A. intermedia and the invasive annual grass B. madritensis was 20% lower (p <

0.05) in both genders of the pepper tree when compared to the coconut mulch and control

(no mulch; Figure 2A, 2D).

Phacelia ramosissima was the only species for which the root and shoot growth

per individual was highest in the control (no mulch) treatment and lowest in the coconut,

female, and male mulch (p < 0.05; Figure 3C, 4C). Although the shoot emergence of A.

intermedia and B. madrentensis was reduced by more than 20% in the pepper tree

mulches (Figure 2A, 2D), there was no reduction in root or shoot biomass. Per individual,

only B. madritensis was significantly different (p < 0.05), with seedlings in male mulch

producing the highest root biomass per individual (Figure 3D). The shoot biomass per

individual was significantly greater in the male mulch for A. intermedia, B. nigra, B. madritensis, and S. pulchra (p < 0.05; Figure 4A, B, D, and E). The root and shoot biomass of S. marianum did not differ amongst treatments (Figure 3F, 4F).

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Soil Experiment

The shoot emergence of A. intermedia was delayed in the pepper soils initially,

however, it did not differ with soil type after seven weeks (Figure 5A). The percent shoot

emergence of B. nigra and P. ramosissima was highest in the pepper tree soils compared

to the control, but not significantly different (Figure 5B, 5C). Compared to the control

soil, the shoot emergence of the annual invasive grass B. madritensis was 34% lower in

the male soil (p < 0.05; Figure 5D). Similarly, the native bunchgrass S. pulchra was 17%

lower (p < 0.05) in the female soil when compared to the control (Figure 5E). The shoot

emergence of S. marianum did not differ in all soil types but was delayed in the pepper

trees soil at the beginning of the experiment (Figure 5F).

Root biomass per individual was only significantly different (p < 0.05) for B.

madritensis, which was highest in the soil from under male trees (Figure 6D). Shoot

biomass per individual was significantly different (p < 0.05) for A. intermedia, which had a lower biomass in female soil compared to the male and control soil (Figure 7A). The shoot biomass of B. nigra was significantly different (p < 0.05) and highest in the male and female soil compared to the control (Figure 7B). Additionally, the root and shoot biomass of P. ramosissima was highest in the female soil but was not significantly different (Figure 6C, 7C). The root and shoot biomass of the S. marianum and S. pulchra did not differ amongst all soil types.

Soil moisture

Soil covered by both genders of the pepper mulch led to greater moisture content when compared to the coconut and control treatments (Figure 8). The control and coconut

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treatment where consistently dryer, evidenced by the lowest readings at or below 0.25 m3m-3 throughout the seven-week mulch trial conducted for B. nigra and P. ramosissima.

Field Observations

The annual invasive grass Bromus diandrus dominated the understory of Q.

agrifolia and was also abundant in the open transects with no canopy cover (Table 3).

While Bromus spp. were generally present beneath pepper trees and oaks, they were smaller in height and more sporadic than populations in the open. Fourteen forb species where identified beneath male and female pepper trees (Table 3). The non-native forb,

Marrubium vulgare was abundant at the dripline and inner canopy of male and female pepper trees. No cactus species where found near the drip line of pepper trees surveyed; however, Opuntia littoralis was present in one oak woodland site (Table 3).

Non-native forbs and grasses occurred beneath both genders of the pepper tree

(Table 3); as well as Stipa lepida, a native perennial bunch grass, and the native forb P. ramosissima, both of which also occurred under oaks. Eleven native were identified in the transects for male and female pepper trees (Table 3). Most shrubs were present at the drip line of the pepper tree with one to three mature shrubs near the trunk where they were usually shaded by dense canopy. The native trees Sambucus mexicana and Juglans californica were present near the dripline of pepper trees in one location

(Table 3). One of the most abundant species underneath pepper trees was the native vine

Marah maricopa, which is abundant in oak woodlands and coastal sage scrub.

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DISCUSSION

This first objective of this study was to determine the potential role of Schinus molle in the restoration of native flora in Southern California. The second was to determine whether Schinus molle exhibited differential allelopathy and a legacy effect amongst genders. Unlike one previous study, during which five of six succulents tested had reduced shoot emergence and biomass when exposed to leaf litter and soil of male pepper trees (Avendaño-González et al., 2016), the forbs and grasses were not affected prominently by the male S. molle mulch in this study. Amsinkia intermedia was the only species negatively affected by female mulch and soil in terms of shoot emergence and root and shoot mass (Table 1, 2). Male pepper tree mulch actually stimulated shoot growth for A. intermedia, B. nigra, B. madritensis, and S. pulchra (Table 1). Silybum marianum was the only species that was not affected by any of the mulch or soil treatments (Table 1, 2), which agrees with another study wherein the female extracts of S. molle did not affect the germination of S. marianum in-vitro (Saad & Abdelgaleil, 2014).

Aside from the negative impacts female S. molle mulch and soil had on A. intermedia; both native and non-native species in this study can germinate and attain comparable biomass when exposed to S. molle mulch and soil.

The literature documenting the allelopathy of S. molle comes from trials conducted on crops and associated weeds (Anaya & Gómez-Pompa, 1971; Borella et al.,

2011; Materechera et al., 2008; Zahed et al., 2010). A group of terpenes and sesquiterpenes extracted from the fruits of S. molle are believed to be the allelochemicals that caused a reduction of the mitotic cell index of lettuce (Lactuca sativa) and onion seedlings (Allium cepa) (Pawlowski et al., 2012). In the present study, the six species

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tested did not experience the same degree of reduction in germination and biomass found in previous studies. While the understory of S. molle in the San Luis Potosi region of

Mexico is reported to have low plant diversity (Avendaño-González et al., 2016), in the present study, 31 plant species (Table 3) beneath 12 pepper trees (6 male trees + 6 female trees = 12 trees) were identified in three locations (Figure 1). The competition for light, however, might better explain the lack of cover below the canopy as noted in previous pepper tree research (Donnelly et al., 2008; Iponga et al., 2008). Prior to this study, no literature had documented allelopathic effects of S. molle in Southern California plant communities. Nor had any study determined if S. molle out-competes plant species for light. In the Karoo region of South Africa, S. molle starves native trees of light leading to greater branch die-off (Iponga et al., 2008; Iponga et al., 2010). Whereas forbs and grasses that could associate beneath the canopy of S. molle were the focus of this study,

11 native shrubs and two trees were identified in field transects (Table 3). Future research needs to first assess the germination and growth of native woodland (trees and shrubs) in the presence of S. molle. Secondly, determine if they are susceptible to greater branch die-off as observed in South Africa. Independent of the negative effects S. molle has on plant species, whether it be allelopathic or a result of deep shade, this species has ability to invade native habitats in Southern California.

On Catalina Island and Channel Islands National Park (CINP), S. molle was selected for preemptive control to mitigate the displacement of Q. agrifolia (J. Knapp,

2010; J. J. Knapp et al., 2009). Between 2008-2011, 243 separate populations of female pepper trees, over 89% of total the population, was removed leaving only males on Santa

Cruz Island of CINP (Cory & Knapp, 2014). Because pepper trees are dioicous, males

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cannot contribute to recruitment without females and by keeping male plants, there is a low probability of a weed shift. As the present study demonstrated, the invasive plants B. nigra and B. madritensis were stimulated by male pepper tree mulch and soil (Table 1, 2).

Thus, the first potential role of S. molle in native plant restoration is the introduction of

shade tolerant plants beneath existing males and the control or removal of females to

inhibit recruitment.

Despite significant reductions in shoot emergence of P. ramosissima in female

mulch (Table 1), the perennial forb accounted for 23% of female and 13% of male pepper

tree cover (Table 3). Phacelia ramosissima and S. molle were in close association

throughout the Carbon Creek area surveyed in the Chino Hills State Park (Figure 1).

Stipa lepida (Foothill needle grass), a native bunch grass comprised 13% of male pepper

tree cover (Table 3), having only been sited beneath pepper trees in the Puente Hills

Landfill Habitat Preserve. Despite the dominant presence of the invasive grass B.

diandrus in all transects both, P. ramosissima and S. lepida were the dominant cover

beneath S. molle. However, further studies need to determine if the association of P. ramosissima, S. lepida, and S. molle are site specific. Phacelia ramosissima and S. lepida along with one native vine (Marah macrocarpus) were also present beneath Q. agrifolia

(Table 3) in both locations. Schinus molle, therefore, provides shade for native species that would otherwise occupy the understory of Q. agrifolia and can be used in restoration.

Whereas female pepper trees can be removed from remote islands of Southern

California without the likelihood of reintroduction, mainland habitat preserves such as those in this study border residential communities. In Southern California, previous studies suggested coyotes (Canis latrans) and avian fauna are dispersing S. molle from

16

urban forests into native habitats (Howard & Minnich, 1989; Nilsen & Muller, 1980), making the control of pepper trees in urban areas ever more difficult. Throughout the fall and winter of 2017-2018 urban forestry technicians were seen pruning residential pepper trees near all three field locations at times removing the entire canopy. In South Africa, residential surveys showed most home owners who had S. molle on their property were unware it was classified as invasive (Shackleton & Shackleton, 2016). Developing an urban forestry campaign to educate the public and advocate for the control of female pepper trees in residential communities near sensitive habitats would reduce the likelihood of dispersal.

In Florida, aggressive pruning to reduce the quantity of viable seeds is one effective tool against the spread and release of allelochemicals produced by Schinus terebinthifolius (Cuda et al., 2006; Nickerson & Flory, 2015). To prevent germination of

S. molle in this study seeds were crushed by hand; in another study seeds were ground into powder mechanically (Materechera et al., 2008). In the same study access to machinery required to process S. molle into an effective allelopathic herbicide was the limiting factor in implementing their method amongst rural farmers. Similarly, hand crushing in this study was not seen as a viable option for implementation rather a method to prevent germination while investigating potential allelopathy. For restoration managers, using female mulch would likely lead to dispersal. However, one study demonstrated S. terebinthifolius had the most allelopathic effect on itself, as male trees inhibited the germination of its own species in growth chamber experiments (Nickerson

& Flory, 2015).

17

The advantage of using both male and female mulch would be to increase the chemical inhibition to suppress invasive plant species such as B. madritensis. In this study, the annual invasive grass had lower shoot emergence in S. molle mulch. Moreover, the shoot emergence of S. pulchra was not affected by pepper tree mulches and had a greater shoot biomass in both genders compared to the control and coconut mulch (Table

1, 2). As a perennial, S. pulchra also flowers long after annual grasses like B. madritensis complete seed production. It should also be noted in this study both pepper tree mulches were visually indistinguishable after 50 days; however, it is unknown whether any allelochemicals remained or were volatized or leached out. In future field studies, the application of pepper tree mulch could suppress the germination of B. madritensis, potentially reducing competition for S. pulchra. Additionally, the pepper tree mulch retained soil moisture (Figure 8) just as well as the coconut and control in this study, which would insulate S. pulchra in dry periods (Fitch, 2017). The female mulch, although effective, is not necessary for the suppression of the invasive grasses, giving male mulch a potential role in restoration.

18

CONCLUSION

As Southern California experienced a prolific die-off of woodland vegetation during the 2012-2015 drought (Jacobsen & Pratt, 2018), soil moisture and shade will be vital to the success of restoration. Recent studies suggest the average precipitation of

California will not change dramatically but will continue to be punctuated by extreme periods of dryness (2012-2015) and deluge (2016-2017) (Berg et al., 2015; Swain et al.,

2018). In South Africa, future precipitation models predict S. molle will persist despite drier conditions (Richardson et al., 2010). Evolving in the Atacama Desert of Peru

(Paredes, 2018), S. molle is adapted to extreme conditions and will likely persist even if

Mediterranean regions become less favorable. In this Southern California study, S. molle did not have the same effects of allelopathy or soil legacy effects as S. terebinthifolius, which has beset restoration efforts in Southern Florida (Donnelly et al., 2008; Morgan &

Overholt, 2005; Nickerson & Flory, 2015). In fact, S. molle may facilitate native understory plant recruitment. This study, therefore, underscores the need of future research to fine-tune the role of both genders in restoration as well as adopting effective management strategies such as those demonstrated in the Channel Islands National Park.

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TABLES AND FIGURES

Figure 1 Maps showing the locations (Chino Hills State Park A, Puente Hills Habitat Preserve B, and the Voorhis Ecological Reserve C) for the transects, each of which included the following: two pepper trees from each gender and two oak trees. The pepper tree material for the greenhouse experiments were collected at the Voorhis Ecological Reserve.

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Table 1 Summary results for the seven-week mulch experiment grouped by species with the mean (± SE) and significant results (p < 0.05) of the Tukey test denoted in bold.

Mulch A. intermedia B. nigra B. madritensis P. ramosissima S. pulchra S. marianum Type Mean ± SE Mean ± SE Mean ± SE Mean ± SE Mean ± SE Mean ± SE Coconut Shoot Emergence 50 ± 0.07 15 ± 3.08 93 ± 0.03 76 ± 4.30 81 ± 0.03 89 ± 0.04 (%) Root Biomass 0.42 ± 0.15 0.02 ± 0.15 0.40 ± 0.10 0.04 ± 0.01 0.21 ± 0.10 0.14 ± 0.03 (g) Shoot Biomass 0.17 ± .04 0.02 ± .04 0.12 ± 0.02 0.07 ± 0.01 0.08 ± 0.02 0.23 ± 0.02 (g) Control Shoot Emergence 58 ± 0.04 23.8 ± 7.22 90 ± 0.03 33 ± 6.04 80 ± 0.05 80 ± 0.07 (%) Root 0.37 ± 0.11 .02 ± 0.11 0.27 ± 0.04 0.12 ± 0.01 0.21 ± 0.03 0.27 ± 0.05 Biomass Shoot Biomass 0.19 ± 0.32 0.02 ± 0.03 0.08 ± 0.01 0.12 ± 0.06 .06 ± 0.01 0.18 ± 0.04 (g) Female Shoot Emergence 23 ± 0.02 20.2 ± 1.39 70 ± 0.03 13 ± 3.00 74 ± 0.03 82 ± 0.04 (%) Root Biomass 0.55 ± 0.13 0.02 ± 0.13 0.50 ± 0.12 0.03 ± 0.03 0.31 ± 0.03 0.29 ± 0.07 (g) Shoot Biomass 0.39 ± .06 0.02 ± .07 0.20 ± 0.04 0.02 ± 0.07 0.15 ± 0.01 0.18 ± 0.04 (g) Male Shoot Emergence 33 ± 0.09 15.4 ± 1.60 72 ± 0.05 44 ± 6.40 84 ± 0.06 84 ± 0.04 (%) Root Biomass 0.48 ± 0.10 0.12 ± 0.10 1.03 ± 0.14 0.12 ± 0.02 0.32 ± 0.04 0.29 ± 0.07 (g) Shoot Biomass 0.69 ± 0.14 0.12 ± 0.14 0.52 ± 0.04 0.02 ± 0.01 0.24 ± 0.2 0.36 ± 0.06 (g)

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Table 2 The summary results for the seven-week soil experiment are grouped by species with the mean (± SE) and significant results (p < 0.05) of the Tukey test denoted in bold.

Soil A. intermedia B. nigra B. madritensis P. ramosissima S. pulchra S. marianum Type Mean ± SE Mean ± SE Mean ± SE Mean ± SE Mean ± SE Mean ± SE Control Shoot Emergence 48 ± 0.04 15.6 ± 2.54 92 ± 0.06 9 ± 3.67 90 ± 0.04 80 ± 0.06 (%) Root 0.07 ± .01 0.04 ± 0.02 0.10 ± 0.02 0.06 ± 0.06 0.11 ± 0.02 0.12 ± 0.04 Biomass Shoot Biomass 0.08 ± .02 0.05 ± 0.01 0.16 ± 0.03 0.05 ± 0.01 0.05 ± 0.01 0.22 ± 0.06 (g) Female Shoot Emergence 32 ± 0.08 31.4 ± 7.01 96 ± 0.04 28 ± 3.67 79 ± 0.04 67 ± 0.04 (%) Root Biomass 0.06 ± 0.04 0.08 ± .01 0.15 ± 0.03 0.17 ± 0.05 0.01 ± 0.04 0.37 ± 0.11 (g) Shoot Biomass 0.02 ± .01 0.25 ± 0.06 0.15 ± 0.04 0.25 ± 0.06 0.04 ± 0.01 0.60 ± 0.12 (g) Male Shoot Emergence 46 ± 0.07 27 ± 3.77 58 ± 0.07 26 ± 8.57 73 ± 0.04 55 ± 0.12 (%) Root Biomass 0.01 ± .06 0.10 ± 0.03 0.22 ± 0.07 0.12 ± 0.05 0.17 ± 0.03 0.40 ± 0.17 (g) Shoot Biomass 0.08 ± 0.01 0.21 ± 0.07 0.17 ± 0.03 0.21 ± 0.07 0.05 ± 0.01 0.60 ± 0.11 (g)

22

Figure 2 The mean (± SE) shoot emergence during the seven-week mulch trial for all six species. Data were reported weekly for all species except B. nigra and P. ramosissima, which were reported every other day. Significant differences for Tukey tests for shoot emergence on the final day of the mulch trial are reported with different letters (p < 0.05).

23

Figure 3 The mean (± SE) root biomass in the mulch trial for all six species. Significant differences on the last day sampled among treatments for Tukey tests are reported with different letters (p < 0.05).

24

Figure 4 The mean (± SE) shoot biomass in the mulch trial for all six species. Significant differences among treatments for Tukey tests (p < 0.05) are reported with different letters.

25

Figure 5 The mean (± SE) shoot emergence of all six species in the seven-week soil trial; data were recorded every other day. Significant differences for the shoot emergence on the final day of the soil trial from the Tukey test (p < 0.05) are reported with different letters.

26

Figure 6 The mean (± SE) root biomass in the soil trial for all six species. Significant differences among treatments for Tukey tests (p < 0.05) are reported with different letters.

27

Figure 7 The mean (± SE) shoot biomass in the soil trial for all six species. Significant differences among treatments for Tukey tests (p < 0.05) are reported with different letters.

28

Figure 8 Volumetric water content in 3 L round pots for each treatment type of the B. nigra and P. ramosissima mulch trial. Data were recorded every other day.

29

Table 3 At three field locations, two transects were recorded beneath the canopies of female and male pepper trees as well as oak trees. Similarly, at each field location two transects had no tree cover (open). The mean (± SE) occurrence of species is reported as percent cover across six transects per cover type for all 47 species identified in 24 transects. Species native to California are dented in bold and species with an asterisk are the six species used in this study.

Species Female Male Oak Open CACTI Opuntia littoralis 2% ± 0.02 13% ± 0.05 FORBS Amsinkia intermedia* 2% ± 0.02 Asclepias fascicularis 4% ± 0.04 Astragalus trichopodus 2% ± 0.02 Brassica nigra* 29% ± 0.06 8% ± 0.04 10% ± 0.04 35% ± 0.07 Carduus pycnocephalus 8% ± 0.04 19% ± 0.06 21% ± 0.06 Centaurea melitensis 4% ± 0.04 25% ± 0.06 23% ± 0.06 Claytonia perfoliata 6% ± 0.05 4% ± 0.04 Conium maculatum 8% ± 0.04 Erodium cicutarium 8% ± 0.04 Galium angustifolium 42% ± 0.07 Hirschfeldia incana 4% ± 0.04 4% ± 0.04 Marrubium vulgare 25% ± 0.06 35% ± 0.07 10% ± 0.04 Medicago polymorpha 4% ± 0.04 Phacelia distans 4% ± 0.04 2% ± 0.02 Phacelia ramosissima* 23% ± 0.06 13% ± 0.05 15% ± 0.05 4% ± 0.04 Pseudognaphalium biolettii 4% ± 0.04 10% ± 0.04 4% ± 0.04 Romneya coulteri 2% ± 0.02 Silybum marianum* 2% ± 0.02 Sonchus asper 2% ± 0.02 2% ± 0.02 2% ± 0.02 2% ± 0.02 Stellaria media 2% ± 0.02 Urtica urens 6% ± 0.05 31% ± 0.07 13% ± 0.05 10% ± 0.04 Solanum americanum 4% ± 0.04 GRASSES Bromus diandrus 25% ± 0.06 25% ± 0.06 69% ± 0.07 75% ± 0.06 Bromus hordeaceus 8% ± 0.04 Bromus madritensis* 13% ± 0.05 6% ± 0.05 48% Stipa lepida 4% ± 0.04 13% ± 0.05 10% ± 0.04 13% ± 0.05 Stipa pulchra* 2% ± 0.02 2% ± 0.02 SHRUBS Artemisia californica 8% ± 0.04 6% ± 0.05 10% ± 0.04 Baccharis pilularis 10% ± 0.04 Baccharis salicifolia 13% ± 0.05 6% ± 0.05 2% ± 0.02 17% ± 0.05 Encelia californica 2% ± 0.02 4% ± 0.04 Encelia farinosa 8% ± 0.04 Eriogonum fasciculatum 4% ± 0.04 2% ± 0.02 13% ± 0.05 Heteromeles arbutifolia 2% ± 0.02 8% ± 0.04 Malosma laurina 6% ± 0.05 6% ± 0.05 Prunus ilicifolia 10% ± 0.04 Rhus integrifolia 4% ± 0.04 Ribes speciosum 4% ± 0.04 Salvia apiana 10% ± 0.04 13% ± 0.05 8% ± 0.04 Toxicodendron diversilobum 2% ± 0.02 6% ± 0.05 TREES Juglans caliornica 4% ± 0.04 8% ± 0.04 4% ± 0.04 Quercus agrifolia 2% ± 0.02 Salix gooddingii 2% ± 0.02 Sambucus mexicana 2% ± 0.02 6% ± 0.05 8% ± 0.04

VINES Cucurbita foetidissima 2% ± 0.02 Marah macrocarpus 27% ± 0.06 42% ± 0.07 35% ± 0.07 13% ± 0.05

30

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